Postcopulatory, Prezygotic Isolation in Flour Beetles
Total Page：16
File Type：pdf, Size：1020Kb
Heredity 72 (1994) 163—167 Received 14 June 1993 Genetical Society of Great Britain Postcopulatory, prezygotic isolation in flour beetles MICHAEL J. WADE*, HAROLD PATTERSONt, NANCY W. CHANG & NORMAN A. JOHNSON Department of Ecology and Evolution, 1101 E. 57th Street, University of Chicago, Chicago, IL 60637 and tHyde Park Career Academy, 6220 S. Stony Is/and, Chicago, IL 60637, USA Wereport the existence of postmating but prezygotic reproductive isolation within flour beetles of the genus Tribolium. Specifically, when a female of either T castaneum or T freemani is paired simultaneously with both a conspecific and a heterospecific male, virtually all of the offspring are sired by the conspecific male. In contrast, when a female of either species is paired only with a heterospecific male, she produces near normal numbers of offspring. Mate choice experiments rule out the possibility that premating reproductive isolation accounts for this phenomenon. A number of different mechanisms could explain this phenomenon of postmating but prezygotic reproductive isolation. Keywords:speciation,postmating reproductive isolation, prezygotic reproductive isolation, mate choice, reinforcement, Tribolium. Introduction hybridization (Brownlee & Sokoloff, 1988; Wade & Johnson, 1993). Theprocess of speciation, the acquisition of genetic Within T. castaneum, mating occurs without elabor- reproductive isolation between populations, is gener- ate courtship and the average copulation duration is ally attributed to the gradual accumulation of genes as 45 s (Park, 1933; Shrode, 1960; Sokoloff, 1974) but a by-product of other adaptive or neutral changes has not been described in T freemani. Both sexes of T occurring in allopatry (Dobzhansky, 1937; Muller, castaneum will mate several times an hour (Park, 1933) 1942; Mayr, 1963; Charlesworth et a!., 1987; Coyne, and males will 'attempt copulation with other males, 1992; Wu & Davis, 1993). Dobzhansky (1940) pre- dead beetles of both sexes, or with any object, such as a sented the 'reinforcement' model, in which natural lump of flour or frass, which looks like a beetle' selection plays a direct role in establishing premating (Sokoloff, 1974, p. 201). Thus, little premating repro- reproductive isolation between populations which have ductive isolation may be expected between these spe- established partial but not complete postmating repro- cies. ductive isolation (presumably by the pleiotropic effects of other adaptive or neutral changes). The importance and methods of the role of reinforcement in natural populations is Materials controversial (Paterson, 1978; Littlejohn, 1981; Butlin, Weused two different T castaneum laboratory strains 1987, 1989; Coyne&Orr, 1989; Howard, 1993). in these experiments: c-SM and c-pl. The c-SM Triboliurn castaneum is a human—commensal flour (castaneum Standard Mixture) was established by M. beetle found worldwide in grain and other stored pro- Wade in 1973 by mass mating 12 males and 12 females ducts. The general biology of this species is summar- from each of the four classic 'Park' T. castaneum stocks ized by Sokoloff (1974). T freemani is a closely related (see Park et al., 1964; Wade, 1976, 1977, for informa- species to T castaneum based on morphological, tion about this strain). It has been maintained in large genetic, karyotypic and molecular data (Hinton, 1948; populations (of more than 1000 breeding adults) ever Sokoloff, 1974; Brownlee & Sokoloff, 1988; Juan et since. This stock also has alleles of an autosomal black a!., 1993). These species are capable of producing body colour locus segregating (Wade & Goodnight, large numbers of viable but sterile F1 progeny on 1991). The c-pl (castaneum pearl) strain has alleles segregating at both the black body colour locus and the *Correspondence pearl eye locus (see Park 1937, for a description of the 164 M. J. WADE ETAL. pearl locus). Only one strain of T freemani was avail- Johnson, 1993). The total of 40 dishes was placed in a able: in this strain there is no variation at any visible darkened incubator at 29°C and observed 28 times markers. over 3 days; the identity of all copulating males was In the simultaneous male experiments, virgin males scored at each observation. The minimum time and females were isolated from T. freemani and the between observations was 20 mm and there were a c-SM strain of T castaneum. Two males and one virgin total of 1120 observations (20 females per species x 2 female were placed into a vial containing 8 g of fine species x 28 observations per female =1120observa- sifted standard medium (by weight, 95 per cent stone- tions). ground whole wheat flour, 5 per cent dried brewers yeast, 0.03 per cent fumagillin; following the protocol Results of Wade & Goodnight, 1991). There were six different treatments, representing all possible combinations of Table1 illustrates the fecundity (numbers of eggs laid), two males (CC, CF, or FF) and a single female (C or F) the hatchability (proportion of eggs hatching) and the and six replicates of each treatment (six treat- larval survival for the simultaneous male treatments. ments Xsixreplicates/treatment =36vials total). Note that the fecundity, hatchability and larval Throughout this paper for the simultaneous male treat- survivorship of a T freemani female mated with two ments, we will use the notation CC-F to indicate that males of her own species (treatment FF-F) is equiva- two T castaneum males were mated to a single T free- lent to that of a T freetnani female mated with two T mani female and similarly for the other five treatments. castaneum males (treatment CC-F). However, the Each vial was fine sifted every 4 days for a total of 28 progeny resulting from the interspecific cross (CC-F) days. At each sift, all eggs were counted and trans- are nearly always sterile or, in rare instances (approxi- ferred to a syracuse dish. The eggs were observed for mately 1 per cent) are weakly fertile, producing a few hatching larvae daily for 8 or 9 days (i.e. until hatching offspring (see also Wade & Johnson, 1993). had ceased). Hatching larvae were censused by repli- When a T. freemani female is simultaneously pre- cate and transferred to a 8 g of regular medium to con- sented with both a conspecific and a heterospecific tinue development. Vials with eggs and larvae were male (treatment CF-F), the fecundity, hatchability and maintained in darkened incubators at 29°C and 70 per larval survivorship are again comparable to those of cent relative humidity throughout the period of egg and the conspecific (FF-F) or interspecific crosses (CC-F) larvae collection. After 45 days, the adult progeny (Table 1). Consequently, in the CF-F treatment, we maturing from each replicate's larval collection was would expect hybrids to constitute approximately half censused. Comparison of larval and adult numbers of the progeny (52.0 per cent, using the product of the permits us to estimate survivorship. relative fitnesses of the FF-F and CC-F treatments). The fertility of the adult progeny of the CC-F, FF-C, The paternity tests of the CF-F progeny (the crosses to CF-C, and CF-F treatments was tested by mating virgin T freemani adults) permit conspecific and individual female progeny with three males from the heterospecific progeny to be discriminated: intra- species of the original mother (e.g. the CC-F female specific progeny are fertile while interspecific progeny progeny were crossed to T freemani males). The male are infertile. Of 191 CF-F offspring test crossed to progeny were individually mated to a single female virgin T freemani adults, only six were sterile. As from the original mother's species. hybrids are nearly always completely sterile, this indi- During the egg collections in the CF-C and CF-F cates that a maximum of 3.1 per cent of CF-F progeny treatments, it was not unusual to find females of both are hybrids (6 of 191). This is more than a 16-fold species engaged in interspecific copulations and copu- difference between the expected and the observed pro- lations were commonly observed in both the CC-F and portions of hybrids (P <0.00001, G-test). (This FF-C treatments. To quantify copulation rates, we estimate is conservative because ancillary data on body observed the copulatory behaviour of 20 females of size and coloration indicate that two of the six sterile each species when presented simultaneously with one beetles were pure T freemani.) male of each species, i.e. 20 additional replicates of There is a similar discrepancy between the observed CF-C and CF-F were set up, each in a petri dish, each and the expected proportions of hybrids in the CF-C containing 1 g of flour. The elytra of the female were treatment. Owing to the differences in fecundity marked with silver paint to distinguish her from the between intraspecific matings (CC-C) and interspecific males and the males of the different species were matings (FF-C) and the lower hatchability of FF-C readily discriminated on the basis of body size differ- eggs, the difference between observed and expected is ences, T freemani being almost three times the mass of smaller in this case but still highly significant T castaneum (Brownlee & Sokoloff, 1988; Wade & (P <0.010, G-test). POSTMATING, PREZYGOTIC ISOLATION 165 Table 1 Fecundity, hatchability and larval survival for the simultaneous male treatments Treatment Fecundity % Hatchability % LarvaI survival males—female Mean S.E. Mean S.E. Mean S.E. T. freemani female FF-F 66.5 9.60 81.07 3.59 89.40 3.48 CF-F 83.3 12.77 85.61 4.60 87.62 3.33 CC-F 73.0 11.49 80.54 4.26 88.65 4.13 T castaneum female CC-C 167.5 20.33 42.69 10.72 77.34 9.01 CF-C 170.5 19.65 41.23 10.82 71.95 6.84 FE-C 64.0 5.46 12.69 2.40 43.33 7.46 In Figure 1, we show time-course patterns of the (a) numbers of eggs laid per female in the different treat- ments.